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Biological Journal of the Linnean Society, 2015, 114, 152–162. With 6 figures
Getting in shape: habitat-based morphological
divergence for two sympatric fishes
KIMBERLY FOSTER1*, LUKE BOWER2 and KYLE PILLER1
1
Southeastern Louisiana University, Department of Biological Sciences, Hammond, LA 70402, USA
Texas A&M University, Department of Wildlife and Fisheries Sciences, College Station, TX 77843,
USA
2
Received 20 June 2014; revised 22 August 2014; accepted for publication 22 August 2014
Freshwater fishes often show large amounts of body shape variation across divergent habitats and, in most cases,
the observed differences have been attributed to the environmental pressures of living in lentic or lotic habitats.
Previous studies have suggested a distinct set characters and morphological features for species occupying each
habitat under the steady–unsteady swimming performance model. We tested this model and assessed body shape
variation using geometric morphometrics for two widespread fishes, Goodea atripinnis (Goodeidae) and Chirostoma
jordani (Atherinopsidae), inhabiting lentic and lotic habitats across the Mesa Central of Mexico. These species were
previously shown to display little genetic variation across their respective ranges. Our body shape analyses reveal
morphometric differentiation along the same axes for both species in each habitat. Both possess a deeper body
shape in lentic habitats and a more streamlined body in lotic habitats, although the degree of divergence between
habitats was less for C. jordani. Differences in the position of the mouth differed between habitats as well, with
both species possessing a more superior mouth in lentic habitats. These recovered patterns are generally consistent
with the steady–unsteady swimming model and highlight the significance of environmental forces in driving
parallel body shape differences of organisms in divergent habitats. © 2014 The Linnean Society of London,
Biological Journal of the Linnean Society, 2015, 114, 152–162.
ADDITIONAL KEYWORDS: atherinopsids – goodeids – morphometrics – phenotypic plasticity – swimming
model.
INTRODUCTION
An important area of interest in evolutionary biology
is the relationship between phenotypes and heterogeneous environmental gradients. At the population
level, morphological trait divergence is the product of
genetic differentiation and phenotypic plasticity via
natural selection (Robinson & Wilson, 1994; Schluter,
2000; Franssen et al., 2013). Selection acts on phenotypes that promote population persistence and
resource utilization (e.g. trophic characters, locomotor
aptitudes, competition, and predation) leading to morphological divergence (Brönmark & Miner, 1992; Day,
2000; Hendry, Taylor & McPhail, 2002; Langerhans,
2008).
Phenotypically divergent populations in heterogeneous environments can arise via divergent selection
*Corresponding author. E-mail: [email protected]
152
on labile traits (Agrawal, 2001; Tobler et al., 2008).
This is particularly true in the aquatic environment,
which is highly variable both from spatial and temporal perspectives. The ability of a fish to move efficiently through water is highly dependent on its body
shape, thereby limiting species to certain habitats or
environmental gradients (Sfakiotakis, Lane & Davies,
1999; Triantafyllou, Triantafyllou & Yue, 2000;
Müller & Van Leeuwen, 2006; Langerhans & Reznick,
2009). Phenotypic responses to flow velocity can be
summed up as the interplay of trade-offs in steady
and unsteady swimming. Steady swimming, the constant locomotion in a straight line (Langerhans,
2008), is necessary in high-flow environments because
of an increase in hydrometric drag, which favours
a streamlined body shape. Alternatively, low-flow
environments correlate with unsteady swimming,
where there are locomotion patterns with inconsistent
changes in direction or velocity, often resulting in a
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 152–162
HABITAT-BASED MORPHOLOGICAL DIVERGENCE
deepened body shape (Brönmark & Miner, 1992;
Hendry et al., 2002; Langerhans, 2008; Franssen,
2011). These traits in concordance with flow differences can result in divergent character selection of
adaptive phenotypes (Langerhans, 2008).
As a result, Langerhans (2008) and, subsequently,
Langerhans & Reznick (2009) proposed a steady–
unsteady swimming performance model to predict
the impacts of natural selection on morphology and
locomotion abilities for fishes inhabiting different flow
regimes. The prediction is based on the idea that
morphology is strongly linked to swimming ability in
fishes and this idea has been supported by many
other studies examining the relationship between
form and function (Webb, 1982, 1984; Sfakiotakis
et al., 1999). The model predicts that fishes occupying
habitats that require steady swimming (i.e. lotic
habitats) should possess morphological features that
enhance swimming performance in these habitats
such as streamlined bodies, shallow/narrow caudal
peduncle, and higher aspect-ratio caudal fins. The
second portion of the model predicts that fish inhabiting low-flow environments (i.e. lentic habitats)
should possess features that enhance unsteady swimming including deeper or larger caudal peduncles,
smaller heads, and lower aspect-ratio caudal fins.
Previous studies comparing body shapes of lentic
and lotic fish populations have found substantial
differences in shape between fishes in these habitats
(Walker, 1997; Hendry et al., 2002; McGuigan et al.,
2003; Langerhans, 2008; Krabbenhoft, Collyer &
Quattro, 2009; Schaefer, Duvernell & Kreiser, 2011;
Webster et al., 2011; Franssen et al., 2013). Additional
biotic and abiotic components of habitats play a
role in differing body shapes and have been shown to
impact fitness and functional success, such as
resource and foraging requirements, predator avoidance, and character displacement as a result of competition (Brönmark & Miner, 1992; Robinson &
Wilson, 1994; Adams & Huntingford, 2004; Svanbäck
et al., 2008). Recently, morphological shape divergence has been shown in anthropogenically altered
habitats of freshwater fish (Haas, Blum & Heins,
2010; Franssen, 2011; Franssen et al., 2013). Therefore, understanding how populations adapt to different habitats may provide an insight into the
consequences of anthropogenic stream modifications
and the evolutionary process.
Central Mexico is relatively depauperate from an
ichthyological perspective (Miller, Minckley & Norris,
2005). The region is dominated by two distantlyrelated fish groups, the New World Silversides
(Atherinopsidae) and the Splitfins (Goodeidae),
which diversified in the region. Silversides (genus
Chirostoma) diversified within the last 0.52 Myr and
occur in both lentic and lotic habitats but reach their
153
greatest diversity in the Central Mexican Lakes
(Barbour, 1973; Bloom et al., 2013). The Mesa Silverside, Chirostoma jordani (Atherinopsidae), is one of
the most widely distributed species in Central
Mexico, occurring in the Ríos Lerma, Grande de Santiago, Panuco, Cazones, Tecolutla, and Ameca, and
the isolated populations in the Rio Mezquital and
Laguna Santiaguilla basins, as well as numerous
inland lakes including (but not limited to) Lakes
Chapala, Cuitzeo, and Patzcuaro, and the endorheic
Valle de México (Fig. 1) (Barbour, 1973; Miller et al.,
2005). The Splitfins (Goodeidae) are comprised of
two subfamilies, EmPetrichthynae and Goodeinae; of
those, Goodeinae is more diverse, containing approximately 42 species that have diversified since the
middle Miocene (Doadrio & Domínguez-Domínguez,
2004). Many species are restricted to a particular
drainage basin or spring habitat but at least one
species, the Tiro or Blackfinned Goodea (Goodea
atripinnis), is widespread throughout the region
occurring in the Ríos Lerma-Grande de Santiago,
Ameca, Balsas, Armeria, the endorheic Lago de
Magdelana basin, and inland lakes on the Mesa
Central (Miller et al., 2005).
Chirostoma jordani and G. atripinnis are generalists in terms of their habitat occupancy because
both species occur in lentic and lotic habitats (Miller
et al., 2005). Furthermore, previous studies have
indicated that both species display limited genetic
variation across their respective ranges (Doadrio &
Domínguez-Domínguez, 2004; Bloom et al., 2009;
K. R. Piller, unpubl. data). This situation offers
the unique opportunity to investigate body shape
differences of two sympatric species with limited
genetic structure across a habitat gradient and to test
hypotheses with regard to divergent selection, which
can drive micro-evolutionary change within species.
First, we hypothesize that there will be differences
in body shape between lentic and lotic habitats
for populations of C. jordani (Atherinopsidae) and
G. atripinnis (Goodeidae) as a result of divergent
selection pressures of these habitats. Second, we the
test the steady–unsteady swimming hypothesis of
Langerhans (2008) and hypothesize that populations
inhabiting lotic environments will be more fusiform
and streamlined in overall body shape relative
to populations occupying lentic waters, thereby
optimizing the locomotion abilities of populations
inhabiting these divergent environments.
MATERIAL AND METHODS
GEOMETRIC MORPHOMETRICS
We examined the shape variation for 178 individuals
of C. jordani and 189 individuals of G. atripinnis from
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 152–162
154
K. FOSTER ET AL.
Figure 1. Map of the distribution of Goodea atripinnis (circles) and Chirostoma jordani (triangles). Small symbols
correspond to vouchered museum records (http://www.fishnet2.org; June 2014). Large symbols correspond to the location
of museum specimens used in the analysis.
both lotic (i.e. rivers, streams, creeks) and lentic (i.e.
lakes, reservoirs) habitats from central Mexico using
museum specimens (see Supportiing information,
Tables S1, S2). The specimens used in the present
study were collected during two general time periods:
1960s and 2000s. We tested for age-related effects and
found no significant differences in body shape and so
all specimens were combined in subsequent analyses.
Based on definitions by Wetzell (2001), a lotic system
is defined as a body of water with unidirectional
water movements along a slope in response to gravity.
In the case of the present study, this includes rivers,
streams, and creeks. A lentic body of water is defined
as a system with still or calm water, although there
may be water movement by mechanisms other than
gravity. These types of bodies of water include lakes,
ponds, presas (reservoirs), and spring pools. The body
shape of C. jordani and G. atripinnis was quantified
using a geometric morphometric approach. The
left lateral side of all specimens was photographed
using a Nikon SLR digital camera. In the family of
Goodeidae, the adult range is from 50 mm standard
length (Webb et al., 2004) and specimens smaller than
50 mm were considered as juveniles. For C. jordani,
Olvera-Blanco et al. (2009) reported that both males
and females reach maturity by one year of age;
this corresponds to approximately 50 mm standard
length. Any juveniles were excluded from the study to
reduce any possible biases due to ontogenetic effects.
Additionally, any damaged or warped specimens were
removed from all analyses. TPSDIG2 (Rohlf, 2005)
was used to digitize twelve homologous landmarks
(Fig. 2). Standard length was measured with calipers
to the nearest 0.1 mm for each specimen. Procrustes
superimposition was used to remove position, orientation, and size biases for each species separately, and
was carried out using MORPHOJ 1.05f (Klingenberg,
2011). Each species aligned data will be referred to as
the ‘shape data’.
MULTIVARIATE
ANALYSIS
To correct for possible allometric shape variation
within species, a pooled within habitat allometric
regression between the shape data and log centroid
size was performed in MORPHOJ 1.05f (Klingenberg,
2011; Sidlauskas, Mol & Vari, 2011). Canonical variate
analysis (CVA) was run in MORPHOJ 1.05f using the
residuals from allometric regression to control for any
allometric shape variation. CVA was used find the
shape features that best distinguish between the
two habitat types. To reduce data dimensionality, a
principal component analysis (PCA) was run using
the residuals of the allometric regression without
further pooling (Sidlauskas et al., 2011). Each species
was analyzed separately. Separate nonparametric
multivariate analysis of variance (NP-MANOVA)
for each species were used to test for significant
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 152–162
HABITAT-BASED MORPHOLOGICAL DIVERGENCE
155
Figure 2. A, geometric landmarks for Goodea atripinnis (1) anterior tip of the snout, (2) posterior aspect of the
neurocranium, (3) anterior origin of the dorsal fin, (4) posterior insertion of the dorsal fin or spiny fin dorsal fin, (5) dorsal
insertion of the caudal fin, (6) ventral insertion of the caudal fin, (7) posterior insertion of the anal fin, (8) anterior
insertion of the anal fin, (9) origin of pelvic fin, (10) the insertion of the operculum on the profile, (11) upper insertion of
the pectoral fin, (12) lower insertion of the pectoral fin. B, geometric landmarks for Chirostoma jordani, (1) tip of snout,
(2) anterior border of epiphyseal bar at midline dorsal neurocranium, (3) origin of first dorsal fin, (4) insertion of second
dorsal fin, (5) dorsal base of caudal fin, (6) ventral base of caudal fin, (7) insertion of anal fin, (8) origin of anal fin,
(9) origin of pelvic fin, (10) intersection of gill opening and ventral body margin, (11) origin of pectoral fin, (12) insertion
of pectoral fin.
differences in the distribution of habitat groups (lentic
and lotic) for all populations in morphospace because
the assumptions of multivariate normal were not
met. NP-MANOVA is an equivalent design to an
ANOVA, allowing the testing of multiple factors and
interactions, but allows for relaxed assumptions by
relying on a permutation procedure (Anderson, 2001).
The NP-MANOVA model included the PC axes that
accounted for > 80% of the variation as the dependent
variables with habitat type (to test the lentic versus
lotic effect) as the fixed effects. Goodeids are sexually
dimorphic; therefore, the effect of sex was tested for as
well. The interaction between the sex and habitat
factors was found to be significant and so a separate
analysis for both sexes was implemented. The
NP-MANOVA was carried out in R software using the
vegan package (R Development Core Team, 2011;
Oksanen et al., 2013). To examine the shape changes
between specimens found in lentic and lotic habitats
for each species, thin spline plates were created from
the residuals of the allometric regression for each
habitat type (lentic versus lotic).
RESULTS
The PCA of the allometric regression residuals
summarized 81.2% of the variation for C. jordani
in the first seven PC axes and 83.3% of the variation
in the first six PC axes for G. atripinnis. Using
NP-MANOVA, morphological divergence was detected
for the habitat variable for C. jordani (Table 1).
When testing for morphological divergence, all variables had a significant effect on body shape variation
for G. atripinnis (Table 1). A significant interaction between sex and habitat type was found for
G. atripinnis, although the results from both sex
match the pooled analysis (see Supporting information, Figs S1, S2; Table S3).
Because only two habitat types were examined, only
one CV axis could be extracted from the CVA. The CVA
plots show distinct habitat groups for both species with
only a few individuals overlapping between groups for
each species (Figs 3, 4). Dorsal fin position, pectoral fin
position, anal fin, pelvic fin position, mouth position,
and caudal peduncle length were characterized as the
most important shape variables for distinguishing the
lotic and lentic specimens for C. jordani (Table 2). In
G. atripinnis, the shape features that best explain the
difference between habitat types were caudal peduncle
length, anal fin, head size, mouth position, and dorsal
fin position (Table 3).
Specimens of C. jordani from lentic habitats had
a more superior mouth, a reduced caudal peduncle,
elongate anal fin, and a deeper body shape (Fig. 5A).
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 152–162
156
K. FOSTER ET AL.
Table 1. Results of the nonparametric multivariate analysis of variance for the species-specific body shape divergence in
lentic and lotic habitats using the PC axes that capture > 80% of the variation for each species. Both sexes were pooled
for G. atripinnis. Effect terms are ranked by the relative variance explained in each model
Species
Model
F value
r2
P value
Chirostoma jordani
Goodea atripinnis
Habitat
Habitat
Sex
Habitat × Sex
12.316
69.187
8.105
6.135
0.066
0.268
0.031
0.024
< 0.001
< 0.001
< 0.001
< 0.001
Figure 3. A plot of the canonical variate (CV) analysis results for Chirostoma jordani, with the CV scores of specimens
on the x-axis and the frequency of the individuals on y-axis.
Specimens from lotic habitats tended to have a more
inferior mouth, longer caudal peduncle, shortened
anal fin, and compressed body shape (Fig. 5B). Individuals of G. atripinnis from the lentic sites were
characterized by a deeper body, shortened head, a
more superior mouth, anteriorly positioned anal and
dorsal fin, and wider, elongated caudal peduncle,
whereas individuals collected from lotic sites had
shallower body, an elongated head, a more inferior
mouth, posteriorly positioned anal and dorsal fin, and
a short, narrow caudal peduncle (Fig. 6).
DISCUSSION
Habitat-associated morphological divergence is common in fishes (Walker, 1997; Hendry et al., 2002;
McGuigan et al., 2003; Langerhans, 2008; Tobler
et al., 2008; Krabbenhoft et al., 2009; Schaefer et al.,
2011; Webster et al., 2011). The results of the present
study demonstrate morphological divergence for
two distantly-related species in two contrasting habitats and support the steady–unsteady swimming
performance model of Langerhans (2008). Both
G. atripinnis and C. jordani independently show a
morphological shift towards a fusiform body shape in
lotic systems, demonstrating similar phenotypic
responses to similar environmental gradients and
flow regimes, despite the lack of intraspecific genetic
variation across their respective ranges (Doadrio &
Domínguez-Domínguez, 2004; Bloom et al., 2009; K.
R. Piller, unpubl. data
The two study species exhibit possible adaptive
responses to divergent habitats, including mouth
position, dorsal fin position, anal fin position, and
caudal peduncle (length and width). Divergent selection pressure is considered to be a major driving force
behind intraspecific polymorphism (Svanbäck et al.,
2008). At least two mechanisms can explain morphological divergence among populations: (1) phenotypic
plasticity, the existence of a range of phenotypes
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 152–162
HABITAT-BASED MORPHOLOGICAL DIVERGENCE
157
Figure 4. A plot of the canonical variate (CV) analysis results for Goodea atripinnis, with the CV scores of specimens on
the x-axis and the frequency of the individuals on y-axis.
under different environmental conditions from a
single genotype, and (2) genetic differentiation, in
which the underlying genetic differences in individuals will be reflected by the phenotype of an individual
(Stearns, 1989). The morphological responses as a
result of phenotypic plasticity may allow for rapid
responses to a changing environment (Robinson &
Wilson, 1994; Crispo, 2008). Predicting such phenotypic plasticity is important for understanding
the impacts of natural or anthropogenic ecosystem
changes on organisms, and may allow for better risk
protection of aquatic ecosystems (Maxwell et al.,
2014). The morphological differences might have
arisen as a result of divergent selection pressures of
water flow differences, dissolved oxygen variation, or
prey type/abundance variation between lotic and
lentic habitats (Crispo & Chapman, 2010; Kekäläinen
et al., 2010; Collin & Fumagalli, 2011).
Numerous biotic and abiotic factors have been
shown to contribute to morphological divergence
(Reznick & Endler, 1982; Reznick et al., 1997;
Langerhans et al., 2003; Krabbenhoft et al., 2009)
for a variety of fishes, including but not limited
to characids (Langerhans et al., 2003), cichlids
(Langerhans et al., 2003), cyprinids (Haas et al.,
2010), poeciliids (Hankison et al., 2006), and
atherinopsids (Krabbenhoft et al., 2009). Lotic environments tend to select for body shapes that reduce
drag because a fusiform shape reduces resistance
in aquatic environments, allowing effective propulsion
and maintenance of velocity at a lower energy
cost (Webb, 1984; Langerhans, 2008; Langerhans
& Reznick, 2009). In the present study, both
G. atripinnis and C. jordani exhibit a more fusiform
body shape in lotic habitats (Figs 5B, 6B, Table 1).
However, the morphological shifts between habitats
are much more apparent in G. atripinnis than
C. jordani (Table 1). This is possibly a result of the
natural streamlined body shape of C. jordani because
similar body shape differences have been recovered
for other species of silversides in other divergent
habitats (O’Reilly & Horn, 2004; Fluker, Pezold &
Minton, 2011). In accordance with the steady–
unsteady performance model of Langerhans (2008), a
more fusiform shape and a narrow caudal peduncle
enhance steady swimming. Both G. atripinnis and
C. jordani had narrower caudal peduncles in lotic
habitats, although C. jordani showed a minimal narrowing and elongation of the caudal peduncle.
Differences in prey type and abundance between
lotic and lentic habitats may have given rise to morphological character diversification, such as mouth
position and head size (Figs 5, 6). These traits have
been attributed to differences in prey choice and
feeding orientation within and between many fish
species (Gatz, 1979; Winemiller, 1991; Hendry et al.,
2002; Russo et al., 2008). Chirostoma jordani is primarily a zooplanktivorous species (Moncayo-Estrada,
Lind & Escalera-Gallardo, 2010; Moncayo-Estrada,
Escalera-Gallardo & Lind, 2011), whereas G.
atripinnis is a filter feeder with a diet of zooplankton
and green algae (Miller et al., 2005). Both species
exhibit more of an upturned mouth in lentic environments (Figs 5, 6) and a more superior mouth has
been shown to a trait common in surface feeding
fishes (Winemiller, 1991, 1992). Based on this feature
alone, this suggests C. jordani and G. atripinnis
may be feeding higher in the water column in lentic
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 152–162
158
K. FOSTER ET AL.
Table 2. The effect of habitat on shape was analyzed
using both a permutation analysis of variance for each
landmark coordinate separately and a canonical variate
analysis (CVA) on residual shape data after an allometric
regression against log centroid size for Chirostoma jordani
Landmarks
Canonical
coefficients
F values
r2
P values
x1
y1
x2
y2
x3
y3
x4
y4
x5
y5
x6
y6
x7
y7
x8
y8
x9
y9
x10
y10
x11
y11
x12
y12
−25.166
−11.755
32.998
16.092
−0.402
−38.489
25.732
84.647
−60.230
16.932
35.127
−39.046
25.848
−34.224
−72.408
94.555
39.002
−108.387
−1.633
61.898
−29.587
−52.358
30.719
10.136
0.127
2.334
6.105
12.139
1.582
13.192
0.993
20.897
23.393
6.900
12.759
0.0922
21.795
2.722
45.27
10.089
3.085
41.512
4.606
0.27985
0.547
1.146
13.247
4.980
0.001
0.013
0.034
0.065
0.009
0.070
0.006
0.107
0.118
0.038
0.067
0.001
0.111
0.015
0.206
0.055
0.017
0.192
0.026
0.002
0.003
0.007
0.070
0.028
0.690
0.150
0.011
> 0.001
0.213
> 0.001
0.312
> 0.001
> 0.001
0.011
> 0.001
0.767
> 0.001
0.082
> 0.001
0.003
0.087
> 0.001
0.029
0.613
0.473
0.251
> 0.001
0.020
The raw canonical coefficients based on the CVA of the
allometric regression residuals. The x- and y-coordinates
are given for each landmark and statistically significant
values are indicated in bold.
environments than in lotic environments. The differences in mouth position for C. jordani and
G. atripinnis may be a response to changes in available prey within the divergent environments
(McEachran, Boesch & Musick, 1976; Ellis, Pawson &
Shackley, 1996; Platell, Sarre & Potter, 1997).
Further data on diet and prey abundance for both
species would be necessary to identify whether the
observed changes in mouth and head morphology can
be definitively attributed to prey differences in the
divergent habitats.
Head size variation previously has been shown
to be a phenotypic response to predation pressure
(Walker, 1997; Vamosi & Schluter, 2002; Langerhans
et al., 2004), where fish populations in the presence of
predators exhibited larger caudal regions, smaller
heads, and more elongate bodies (Langerhans et al.,
2004). Such changes may be advantageous for preda-
Table 3. The effect of habitat on shape was analyzed
using both a permutation analysis of variance for each
landmark coordinate separately and a CVA analysis on
residual shape data after an allometric regression against
log centroid size for G. atripinnis. The raw canonical coefficients based on the canonical variate analysis (CVA) of
the allometric regression residuals
Landmarks
Canonical
coefficients
F values
r2
P values
x1
y1
x2
y2
x3
y3
x4
y4
x5
y5
x6
y6
x7
y7
x8
y8
x9
y9
x10
y10
x11
y11
x12
y12
−24.966
13.730
5.255
−59.857
−46.665
38.622
−44.093
−8.986
52.734
48.246
−13.773
−8.449
36.377
−77.416
−46.029
−21.963
44.243
−1.777
70.084
60.772
7.444
19.511
−40.611
−2.437
15.802
44.980
1.6381
0.1283
202.680
60.995
59.052
83.124
45.060
32.550
36.167
37.878
16.620
106.940
80.872
62.047
4.383
6.675
66.357
2.158
11.802
0.2614
0.1969
15.401
0.079
0.196
0.009
0.001
0.523
0.248
0.242
0.310
0.196
0.149
0.164
0.169
0.082
0.366
0.304
0.251
0.023
0.034
0.263
0.011
0.059
0.001
0.001
0.076
0.002
> 0.001
0.193
0.719
> 0.001
> 0.001
> 0.001
> 0.001
> 0.001
> 0.001
> 0.001
> 0.001
> 0.001
> 0.001
> 0.001
> 0.001
0.030
0.009
> 0.001
0.127
0.003
0.630
0.659
> 0.001
The x- and y-coordinates are given for each landmark and
statistically significant values are indicated in bold.
tor evasion because they increase unsteady or burst
swimming as a result of the enlarged musculature in
the caudal region and the smaller, more fusiform
anterior region (Langerhans et al., 2004). Similarly,
the present study found that G. atripinnis displayed a
larger caudal peduncle and shortened, smaller head
in lentic habitats, although testing the effect of predation on body shape would require additional predator data from the field.
Based on the data that we have on hand, it appears
as though phenotypic plasticity is the driving force
behind the morphological divergence observed across
habitats for both species. Gene flow would only constrain morphological adaptation but not phenotypic
plasticity (Scheiner, 1993; Hendry et al., 2002).
However, it is possible that large mixing of populations across habitat types would constrain genetic
diversification and phenotypic plasticity, lessening or
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 152–162
HABITAT-BASED MORPHOLOGICAL DIVERGENCE
159
Figure 5. Transformation grids illustrating the shape changes between a consensus shape of each habitat type and a
mean shape of all specimens, using the residual data for Chirostoma jordani. The lines point in the direction of the shape
change for each landmark, where A denotes specimens collected from lentic habitats and B denotes specimens from lotic
habitats.
Figure 6. Transformation grids illustrating the shape changes between a consensus shape of each habitat type and a
mean shape of all specimens, using the residual data for Goodea atripinnis. The lines point in the direction of the shape
change for each landmark, where A denotes specimens collected from lentic habitats and B denotes specimens from lotic
habitats.
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 152–162
160
K. FOSTER ET AL.
preventing morphological diversification. Neotropical
silversides are an economically important component of Mexican fisheries (Lyons et al., 1998), and
C. jordani is the most widely distributed silverside
species in Central Mexico (Barbour, 1973; Miller
et al., 2005). With regard to C. jordani, the weaker
morphological difference between the lentic and
lotic populations could be attributed to undocumented
introductions of individuals among habitats.
However, further data based on fisheries and the
movement of individuals between habitats would be
necessary to test this hypothesis.
CONCLUSIONS
In summary, the body shape variation observed in the
present study most accurately reflects the steady–
unsteady swimming performance model (Langerhans,
2008; Langerhans & Reznick, 2009). Both species
developed a deeper body shape suitable for unsteady
swimming in lentic environments and streamlined body shapes in lotic habitats. Additionally,
G. atripinnis developed a smaller head size and wider
elongated caudal peduncle in lentic habitats and a
larger head size and shallow/narrow caudal peduncle
in lotic habitats, further supporting the steady–
unsteady swimming performance model (Langerhans,
2008; Krabbenhoft et al., 2009; Langerhans &
Reznick, 2009).
Clearly, the general influence of the different
habitat regimes has played a role in the body shape
differences recovered in the present study and highlights similar adaptive morphological responses
of the two distantly-related sympatric species to
similar environmental gradients. With the lack of
intraspecific genetic variation, phenotypic plasticity is
the likely mechanism for the morphological divergence seen in the present study (Stearns, 1989). The
morphology of head and mouth regions may be
related to differences in prey or environmental differences within each habitat type, although additional
research is needed to disentangle the main driving
forces behind the morphological divergence. Our
results are consistent with the evolutionary hypothesis that divergent habitats drive intraspecific phenotypic diversification, and are important for predicting
adaptive responses of freshwater fish species to divergent habitats and anthropogenic stream modification.
ACKNOWLEDGEMENTS
We would to thank Nelson Rios and Hank Bart (TU)
for the loan of the museum specimens. Additional
samples used in the present study were collected with
the assistance of D. Bloom, J. Lyons, N. MercadoSilva, and P. Gesundheit. We would also like to thank
the anonymous reviewers for their helpful comments.
This study was supported, in part, by an NSF grant
(DEB 0918073) to KRP.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article at the publisher’s web-site:
Figure S1. Thin spline plates using the residuals of the allometric regression for Goodea atripinnis females
with lines pointing in the direction of the shape change for each landmark, where A denotes specimens collected
from lentic habitats and B denotes specimens from lotic habitats.
Figure S2. Thin spline plates using the residuals of the allometric regression for Goodea atripinnis males with
lines pointing in the direction of the shape change for each landmark, where A denotes specimens collected from
lentic habitats and B denotes specimens from lotic habitats.
Table S1. Locality information and habitat designation for Goodea atripinnis (Goodeidae).
Table S2. Locality information and habitat designation for Chirostoma jordani (Atherinopsidae).
Table S3. NP-MANOVA results testing for the species-specific body shape divergence in lentic and lotic
habitats using the matrix of residuals for G. atripinnis.
© 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 152–162